Geographic Mosaic of Extensive Genetic Variations in Subterranean Mole Voles Ellobius alaicus as a Consequence of Habitat Fragmentation and Hybridization

Abstract

Restricted mobility, sociality, and high inbreeding—characteristic for subterranean mammals—lead to rapid changes in their genome structure. Up to now, the Alay mole vole Ellobius alaicus was a data-deficient species; its spatial and phylogenetic relationships with a sibling species, E. tancrei, were not clarified. We carried out a genetic analysis including differential G-banding of chromosomes and mitochondrial (cytb) and nuclear gene (XIST and IRBP) sequencing. The phylogenetic reconstruction based on cytb represented the expected phylogenetic relationships of two species. Using the XIST, we revealed two new lineages among E. alaicus from the Alay Valley (Southern Kyrgyzstan). Analysis of IRBP demonstrated presence of the specific genotype in most of E. alaicus specimens, but also revealed the haplotype, typical for E. tancrei, in some Alay mole voles. The results may be explained as persistence of ancestral gene polymorphism in E. alaicus or limited interspecific hybridization with E. tancrei. Several chromosomal forms were revealed in E. alaicus in the Alay Valley. We propose that ‘mosaic’ genetic polymorphism might appear in E. alaicus due to fragmentation of their habitats in highlands of the Alay Valley, Tien Shan, and Pamir-Alay as well as due to hybridization with E. tancrei or persistence of ancestral polymorphisms.

Nonhomologous Chromosome Interactions in Prophase I: Dynamics of Bizarre Meiotic Contacts in the Alay Mole Vole Ellobius alaicus (Mammalia, Rodentia)

“…All studied E. alaicus specimens had karyotypes with 2n = 52 and NF = 56, as the most previously analyzed Alay mole voles [ 20 , 29 ].…”

“…The result may explain the low effect of negative selection against Rb translocation. Since selection does not eliminate the rearranged chromosomes in meiosis, they have a chance to pass into gametes and survive in natural populations of E. alaicus [ 28 , 29 ].…”

“…Chromatin inactivation was revealed using an anti-γH2AFX antibody (violet). The non-Robertsonian chromosome is designated as 7 according to the karyotype [ 28 , 29 ]. The contact regions of nonhomologous bivalents are localized in the H3K9me3 clouds.…”

“…Such contacts resemble the specialized chromosomal regions in which the short arms of nonhomologous chromosomes extend, contact (‘touching’ type), partly fuse with each other (‘anchoring/tethering’ type), and even follow a pattern of a complete fusion (‘fusion’ type). These findings, and the fact that the Alay mole vole is a species with Robertsonian variability [ 28 , 29 ], allowed us to assume that such meiotic contacts may be a prelude to a Robertsonian translocation and could have taken place in the evolutionary history of this species.…”